Objective. To study the relationship between the brain-derived neurotrophic factor (BDNF) level and the severity of nocturnal hypoxemia in patients in the acute and early recovery periods of ischemic stroke (IS). Materials and methods. The study included 44 patients (27 men and 17 women) aged 18–85 years in the acute phase of IS. A total of 35 patients (21 men and 14 women) were examined at follow-up three months later. During the acute period, routine diagnostic procedures were supplemented with respiratory monitoring and measurement of serum BDNF levels using an enzyme immunoassay method. BDNF levels were also re-evaluated at outpatient visits three months after IS. Neurological status and changes during the acute period of stroke were assessed as part of routine clinical practice using the National Institutes of Health Stroke Scale (NIHSS) on admission and discharge. Results. Weak direct relationships were found between the durations of hypoxemia and saturation levels (SpO2) of <90% (r = 0.327, p = 0.035) and <85% (r = 0.461, p = 0.003) and the BDNF level in the acute period of IS. BDNF levels in the acute period of IS correlated negatively with the minimum saturation value (r = –0.328, p = 0.034). A direct relationship was also demonstrated between the BDNF level in the early recovery period of IS and the duration of hypoxemia with SpO2 <85% (r = –0.389, p = 0.028). Regression analysis results showed that the minimum saturation level is a predictor of the BDNF level. No signifi cant relationships were found with measures of the severity of sleep-disordered breathing such as the apnea-hypopnea index and desaturation index. Conclusions. The severity of nocturnal hypoxemia is associated with increased BDNF levels in both the acute and recovery periods of ischemic stroke, regardless of the presence of concomitant sleep-disordered breathing.
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References
V. L. Feigin, B. A. Stark, C. O. Johnson, et al., ”Global, regional, and national burden of stroke and its risk factors, 1990–2019: A systematic analysis for the Global Burden of Disease Study 2019,” Lancet Neurol., 20, 795–820 (2021), https://doi.org/10.1016/S1474-4422(21)00252-0.
V. I. Ignat’eva, I. A. Voznyuk, N. A. Shamalov, et al., “Socioeconomic burden of stroke in the Russian Federation,” Zh. Nevrol. Psikhiatr., 123, No. 8–2, 5–15 (2023), https://doi.org/10.17116/jnevro20231230825.
G. Kim and E. Kim, “The effects of antecedent exercise on motor function recovery and brain-derived neurotrophic factor expression after focal cerebral ischemia in rats,” J. Phys. Ther Sci., 25, No. 5, 553–556 (2013), https://doi.org/10.1589/jpts.25.5_553.
V. V. Roslavtseva, A. B. Salmina, S. V. Prokopenko, et al., “Possibilities of using brain neurotrophic factor as a marker of therapeutic effi cacy in degenerative, traumatic, and ischemic brain damage,” Nevrol. Zh., 20, No. 2, 38–46 (2015).
A. Navarrete-Opazo and G. S. Mitchell, “Therapeutic potential of intermittent hypoxia: a matter of dose,” Am. J. Physiol. Regul. Integr. Comp. Physiol., 307, No. 10, R1181–R1197 (2014), https://doi.org/10.1152/ajpregu.00208.2014.
M. Chroboczek, S. Kujach, M. Łuszczyk, et al., “Acute normobaric hypoxia lowers executive functions among young men despite increase of BDNF concentration,” Int. J. Environ. Res. Public Health, 19, No. 17, 10802 (2022), https://doi.org/10.3390/ijerph191710802.
N. Cichoń, M. Bijak, P. Czarny, et al., “Increase in blood levels of growth factors involved in the neuroplasticity process by using an extremely low frequency electromagnetic fi eld in post-stroke patients,” Front. Aging Neurosci., 10, 294 (2018), https://doi.org/10.3389/fnagi.2018.00294.
W. Liu, X. Wang, M. O’Connor, et al., “Brain-derived neurotrophic factor and its potential therapeutic role in stroke comorbidities,” Neural Plast., 2020, 1969482 (2020), https://doi.org/10.1155/2020/1969482.
A. Berretta, Y. C. Tzeng, and A. N. Clarkson, “Post-stroke recovery: the role of activity-dependent release of brain-derived neurotrophic factor,” Expert Rev. Neurother., 14, No. 11, 1335–1344 (2014), https://doi.org/10.1586/14737175.2014.969242.
P. Ferdinand and C. Roffe, “Hypoxia after stroke: a review of experimental and clinical evidence,” Exp. Transl. Stroke Med., 8, 1–8 (2016), https://doi.org/10.1186/s13231-016-0023-0.
A. Seiler, M. Camilo, L. Korostovtseva, et al., “Prevalence of sleep-disordered breathing after stroke and TIA: A meta-analysis,” Neurology, 92, No. 7, e648–e654 (2019), Epub 2019 Jan 11, PMID: 30635478, https://doi.org/10.1212/WNL.0000000000006904.
L. Korostovtseva, M. Bochkarev, V. Amelina, et al., “Sleep-disordered breathing and prognosis after ischemic stroke: It is not apnea-hypopnea index that matters,” Diagnostics (Basel), 13, No. 13, 2246 (2023), https://doi.org/10.3390/diagnostics13132246.
Y. Feng, L. Ma, X. Chen, et al., “Relationship between serum brain-derived neurotrophic factor and cognitive impairment in children with sleep-disordered breathing,” Front. Pediatr., 10, 1027894 (2023), https://doi.org/10.3389/fped.2022.1027894.
B. Arslan, R. Şemsi, A. İriz, et al., “The evaluation of serum brain-derived neurotrophic factor and neurofi lament light chain levels in patients with obstructive sleep apnea syndrome,” Laryngoscope Investig. Otolaryngol., 6, No. 6, 1466–1473 (2021), https://doi.org/10.1002/lio2.683.
P. Lyden, “Using the National Institutes of Health Stroke Scale,” Stroke, 48, No. 2, 513–519 (2017), https://doi.org/10.1161/strokeaha.116.015434.
H. Adams, B. Bendixen, L. Kappelle, et al., “Classifi cation of subtype of acute ischemic stroke defi nitions for use in a multicenter clinical trial,” Stroke, 24, 35–41 (1993), https://doi.org/10.1161/01.STR.24.1.35.
R. B. Berry, R. Brooks, C. Gamaldo, et al., “AASM scoring manual updates for 2017 (version 2.4),” J. Clin. Sleep Med., 13, No. 5, 665–666 (2017), https://doi.org/10.5664/jcsm.6576.
R Core Team, A Language and Environment for Statistical Computing [Internet], Vienna, Austria (2023), https://www.R-project.org/.
J. Pinheiro, D. Bates, and R Core Team, nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–164, [Internet] (2023), https://CRAN.R-project.org/package=nlme.
D. M. Pinheiro and J. C. Bates, Mixed-Effects Models in S and S-PLUS [Internet], Statistics and Computing, Springer-Verlag (2000), https://doi.org/10.1007/b98882.
J. Fox and S. Weisberg, An R Companion to Applied Regression, Sage, Thousand Oaks, CA, [Internet] (2019), 3rd ed., https://socialsciences.mcmaster.ca/jfox/Books/Companion/.
H. Wickham, ggplot2: Elegant Graphics for Data Analysis, Springer International Publishing, Cham, Switzerland (2016), 2nd ed.
A. Becke, P. Müller, M. Dordevic, et al., “Daily intermittent normobaric hypoxia over 2 weeks reduces BDNF plasma levels in young adults – A randomized controlled feasibility study,” Front. Physiol., 9, 1337 (2018), https://doi.org/10.3389/fphys.2018.01337.
J. El-Sayes, D. Harasym, C. V. Turco, et al., “Exercise-induced neuroplasticity: A mechanistic model and prospects for promoting plasticity,” Neuroscientist, 25, No. 1, 65–85 (2019), https://doi.org/10.1177/1073858418771538.
T. Casoli, C. Giuli, M. Balietti, et al., “Effect of cognitive training on the expression of brain-derived neurotrophic factor in lymphocytes of mild cognitive impairment patients,” Rejuvenation Res., 17, No. 2, 235–238 (2014), https://doi.org/10.1089/rej.2013.1516.
G. S. Golosnaya, A. S. Petrukhin, A. A. Terent’ev, et al., “Brainderived neurotrophic factor (BDNF) in the early diagnosis of intraventricular hemorrhage and periventricular leukomalacia in newborn infants,” Vopr. Sovremen. Pediatr., 4, No. 3, 13–18 (2005).
Y. Naegelin, H. Dingsdale, K. Säuberli, et al., “Measuring and validating the levels of brain-derived neurotrophic factor in human serum,” eNeuro, 5, No. 2, 23–28 (2018), https://doi.org/10.1523/ENEURO.0419-17.2018.
W. Tao, X. Zhang, J. Ding, et al., “The effect of propofol on hypoxiaand TNF-α-mediated BDNF/TrkB pathway dysregulation in primary rat hippocampal neurons,” CNS Neurosci. Ther., 28, No. 5, 761–774 (2022), https://doi.org/10.1111/cns.13809.
P. Chaturvedi, A. K. Singh, V. Tiwari, et al., “Brain-derived neurotrophic factor levels in acute stroke and its clinical implications,” Brain Circ., 6, No. 3, 185–190 (2020), https://doi.org/10.4103/bc.bc_23_20.
E. Karantali, D. Kazis, V. Papavasileiou, et al., “Serum BDNF levels in acute stroke: A systematic review and meta-analysis,” Medicina (Kaunas), 57, No. 3, 297 (2021), https://doi.org/10.3390/medicina57030297.
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Translated from Zhurnal Nevrologii i Psikhiatrii imeni S. S. Korsakova, Vol. 124, No. 5, Iss. 2, pp. 72–78, May, 2024.
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Zabroda, E.N., Amelina, V.V., Gordeev, A.D. et al. Brain-Derived Neurotrophic Factor in the Acute and Early Recovery Period of Ischemic Stroke: The Role of Nocturnal Hypoxemia. Neurosci Behav Physi (2024). https://doi.org/10.1007/s11055-024-01701-y
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DOI: https://doi.org/10.1007/s11055-024-01701-y